biologia plantarum

International journal on Plant Life established by Bohumil Nìmec in 1959

Biologia plantarum 54:403-414, 2010 | DOI: 10.1007/s10535-010-0075-2

The responsiveness of the IAA2 promoter to IAA and IBA is differentially affected in Arabidopsis roots and shoots by flavonoids

G. Rusak1,*, S. Cerni1, D. Stupin Polancec2, J. Ludwig-Müller3
1 Department of Biology, Faculty of Science, Zagreb, Croatia
2 GSK Research Centre Zagreb, Ltd., Zagreb, Croatia
3 Institut für Botanik, Technische Universität Dresden, Dresden, Germany

The structural features of flavonoids which are involved in the modulation of auxin distribution in Arabidopsis thaliana were evaluated. An auxin-inducible promoter IAA2 fused to a reporter gene (GUS) was used to monitor the tissue responsiveness to auxins. The following aspects were investigated: 1) the influence of flavonoids (quercetin, naringenin, kaempferol, myricetin and isorhamnetin) on the distribution of indole-3-acetic acid (IAA) and indole-3-butyric acid (IBA) in roots and leaves, 2) differences in flavonoid uptake into roots and shoots depending on flavonoid concentration in the medium, and 3) influence of structurally different flavonoids on the gravitropic response and growth of roots. The same flavonoids differently affected IAA and IBA distribution in leaves and roots. There were several structural requirements for the flavonoids which resulted in the changes of auxin response/distribution. Great differences between the ability of shoots and roots to take up quercetin were showed. Also, flavonoids influenced gravitropism and root growth of Arabidopsis seedlings in a structure-dependent manner.

Keywords: isorhamnetin; kaempferol; myricetin; naringenin; phenolics; plant hormones; quercetin
Subjects: Arabidopsis thaliana; auxins; flavonoids; β-glucuronidase; kaempferol; naringenin; polymerase chain reaction (PCR); quercitin; transgenic plants

Received: October 2, 2008; Accepted: June 9, 2009; Published: September 1, 2010  Show citation

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Rusak, G., Cerni, S., Stupin Polancec, D., & Ludwig-Müller, J. (2010). The responsiveness of the IAA2 promoter to IAA and IBA is differentially affected in Arabidopsis roots and shoots by flavonoids. Biologia plantarum54(3), 403-414. doi: 10.1007/s10535-010-0075-2
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References

  1. Bailly, A., Sovero, V., Vincenzetti, V., Santelia, D., Bartnik, D., Koenig, B.W., Mancuso, S., Martinoia, E., Geisler, M.: Modulation of P-glycoproteins by auxin transport inhibitors is mediated by interaction with immunophilins. - J. biol. Chem. 283: 21817-21826, 2008. Go to original source...
  2. Bartel, B., LeClere, S., Magidin, M., Zolman, B.K.: Inputs to the active indole-3-acetic acid pool: de novo synthesis, conjugate hydrolysis, and indole-3-butyric acid β-oxidation. - J. Plant Growth Regul. 20: 198-216, 2001. Go to original source...
  3. Bennett, M.J., Marchant, A., Green, H.G.: Arabidopsis AUX1 Gene: a permease-like regulator of root gravitropism. - Science 273: 948-950, 1996. Go to original source...
  4. Besseau, S., Hoffmann, L., Geoffroy, P., Lapierre, C., Pollet, B., Legrand, M.: Flavonoid accumulation in Arabidopsis repressed in lignin synthesis affects auxin transport and plant growth. - Plant Cell 19: 148-162, 2007. Go to original source...
  5. Brown, D.E., Rashotte, A.M., Murphy, A.S., Normanly, J., Tague, B.W., Peer, W.A., Taiz, L., Muday, G.K.: Flavonoids act as negative regulators of auxin transport in vivo in Arabidopsis. - Plant Physiol. 126: 524-535, 2001. Go to original source...
  6. Buer, C.S., Muday, G.K.: The transparent testa4 mutation prevents flavonoid synthesis and alters auxin transport and the response of Arabidopsis roots to gravity and light. - Plant Cell 16: 1191-1205, 2004. Go to original source...
  7. Buer, C.S., Muday, G.K., Djordjevic, M.A.: Flavonoids are differentially taken up and transported to long distances in Arabidopsis. - Plant Physiol. 145: 478-490, 2007. Go to original source...
  8. Costa, S., Dolan, L.: Development of the root pole and cell patterning in Arabidopsis roots. - Curr. Opin. Genet. Dev. 10: 405-409, 2000. Go to original source...
  9. Davies, P.J.: The plant hormones: their nature, occurrence, and function. - In: Davies, P.J. (ed.): Plant Hormones: Biosynthesis, Signal Transduction and Action. Pp. 1-15. Kluwer Academic Publishers, Dordrecht 2004. Go to original source...
  10. Debeaujon, I., Léon-Kloosterziel, K.M., Koornneef, M.: Influence of the testa on seed dormancy, germination, and longevity in Arabidopsis. - Plant Physiol. 122: 403-414, 2000. Go to original source...
  11. Delker, C., Raschke, A., Quint, M.: Auxin dynamics: the dazzling complexity of a small molecule's message. - Planta 227: 929-941, 2008. Go to original source...
  12. Dharmasiri, S., Swarup, R., Mockaitis, K., Dharmasiri, N., Singh, S.K., Kowalchyk, M., Marchant, A., Mills, S., Sandberg, G., Bennett, M.J., Estelle, M.: AXR4 is required for localization of the auxin influx facilitator AUX1. - Science 312: 1218-1220, 2006. Go to original source...
  13. Dubrovsky, J.G., Sauer, M., Napsucialy-Mendivil, S., Ivanchenko, M.G., Friml, J., Shishkova, S., Celenza, J., Benkova, E.: Auxin acts as a local morphogenetic trigger to specify lateral root founder cells. - Proc. nat. Acad. Sci. USA 105: 8790-8794, 2008. Go to original source...
  14. Epstein, E., Ludwig-Müller, J.: Indole-3-butyric acid in plants: occurrence, synthesis, metabolism and transport. - Physiol. Plant. 88: 382-389, 1993. Go to original source...
  15. Faulkner, I.J., Rubery, P.H.: Flavonoids and flavonoid sulphates as probes of auxin-transport regulation in Cucurbita pepo hypocotyl segments and vesicles. - Planta 186: 618-625, 1992. Go to original source...
  16. Friml, J., Wisniewska, J., Benkova, E., Mendgen, K., Palme, K.: Lateral relocation of auxin efflux regulator PIN3 mediates tropism in Arabidopsis. - Nature 415: 806-809, 2002. Go to original source...
  17. Gälweiler, L., Guan, C., Müller, A., Wisman, E., Mendgen, K., Yephremov, A., Palme, K.: Regulation of polar auxin transport by AtPIN1 in Arabidopsis vascular tissue. - Science 282: 2226-2230, 1998. Go to original source...
  18. Gee, M.A., Hagen, G., Guilfoyle, T.J.: Tissue-specific and organ-specific expression of soybean auxin-responsive transcripts GH3 and SAURs. - Plant Cell 3: 419-430, 1991. Go to original source...
  19. Geisler, M., Murphy, A.S.: The ABC of auxin transport: the role of p-glycoproteins in plant development. - FEBS Lett. 580: 1094-1102, 2006. Go to original source...
  20. Geldner, N., Friml, J., Stierhof, Y.-D., Jürgens, G., Palme, K.: Auxin transport inhibitors block PIN1 cycling and vesicle trafficking. - Nature 413: 425-428, 2001. Go to original source...
  21. Gester, S., Metz, P., Zierau, O., Vollmer, G.: An efficient synthesis of the potent phytoestrogens 8-prenylnaringenin and 6-(1,1-dimethylallyl)naringenin by europium(III)-catalized Claisen rearrangement. - Tetrahedron 57: 1015-1018, 2001. Go to original source...
  22. Grotewold, E., Drummond, B.J., Bowen, B., Peterson, T.: The myb-homologous P gene controls phlobaphene pigmentation in maize floral organs by directly activating a flavonoid biosynthetic gene subset. - Cell 76: 543-553, 1994. Go to original source...
  23. Hagen, G., Martin, G., Li, Y., Guilfoyle, T.J.: Auxin-induced expression of the soybean GH3 promoter in transgenic tobacco plants. - Plant mol. Biol. 17: 567-579, 1991. Go to original source...
  24. Jacobs, M., Rubery, P.H.: Naturally occurring auxin transport regulators. - Science 241: 346-349, 1998. Go to original source...
  25. Jefferson, R.A.: Assaying chimeric genes in plant: the GUS gene fusion system. - Plant mol. Biol. Rep. 5: 387-405, 1987. Go to original source...
  26. Kovaleva, L.V., Zakharova, E.V., Minkina, Yu.V.: Auxin and flavonoids in the progame phase of fertilization in petunia. - Russ. J. Plant Physiol. 54: 396-401, 2007. Go to original source...
  27. Larkin, P.J., Gibson, J.M., Mathesius, U., Weinman, J.J., Gartner, E., Hall, E., Tanner, G.J., Rolfe, B.G., Djordjevic, M.A.: Transgenic white clover. Studies with the auxinresponsive promoter, GH3, in root gravitropism and lateral root development. - Transgenic Res. 5: 325-335, 1996. Go to original source...
  28. Levizou, E., Karageorgou, P., Petropoulou, Y., Grammatikopoulos, G., Manetas Y.: Induction of ageotropic response in lettuce radicle growth by epicuticular flavonoid aglycons of Dittrichia viscose - Biol. Plant. 48: 305-307, 2004. Go to original source...
  29. Ljung, K., Hull, A.K., Kowalczyk, M., Marchant, A., Celenza, J., Cohen, J.D., Sandberg, G.: Biosynthesis, conjugation, catabolism and homeostasis of indole-3-acetic acid in Arabidopsis thaliana. - Plant mol. Biol. 49: 249-272, 2002. Go to original source...
  30. Ludwig-Müller, J., Kaldorf, M., Sutter, E.G., Epstein, E.: Indole-3-butyric acid (IBA) is enhanced in young maize (Zea mays L.) roots colonized with the arbuscular mycorrhizal fungus Glomus intraradices. - Plant Sci. 125: 153-162, 1997. Go to original source...
  31. Ludwig-Müller, J., Sass, S., Sutter, E.G., Wodner, M., Epstein, E.: Indole-3-butyric acid in Arabidopsis thaliana. I. Identification and quantification. - Plant Growth Regul. 13: 179-187, 1993. Go to original source...
  32. Ludwig-Müller, J., Schubert, B., Pieper, K.: Regulation of IBA synthetase from maize (Zea mays L.) by drought stress and ABA. - J. exp. Bot. 46: 423-432, 1995. Go to original source...
  33. Luschnig, C., Gaxiola, R.A., Grisafi, P., Fink, G.R.: EIR1, a root-specific protein involved in auxin transport, is required for gravitropism in Arabidopsis thaliana. - Genes Dev. 12: 2175-2187, 1998. Go to original source...
  34. Marchant, A., Bhalerao, R., Casimiro, I., Eklöf, J., Casero, P.J., Bennett, M., Sandberg, G.: AUX1 promotes lateral root formation by facilitating indole-3-acetic acid distribution between sink and source tissues in the Arabidopsis seedling. - Plant Cell 14: 589-597, 2002. Go to original source...
  35. Marchant, A., Kargul, J., May, S.T., Mulle, P., Delbarre, A., Perrot-Rechenmann, C., Bennett, M.J.: AUX1 regulates root gravitropism in Arabidopsis by facilitating auxin uptake within root apical tissues. - EMBO J. 18: 2066-2073, 1999. Go to original source...
  36. Mathesius, U.: Flavonoids induced in cells undergoing nodule organogenesis in white clover are regulators of auxin breakdown by peroxidase. - J. exp. Bot. 52: 419-426, 2001. Go to original source...
  37. Muday, G.K., DeLong, A.: Polar auxin transport: controlling where and how much. - Trends Plant Sci. 6: 535-542, 2001. Go to original source...
  38. Muday, G.K., Murphy, A.S.: An Emerging Model of Auxin Transport Regulation. - Plant Cell 14: 293-299, 2002. Go to original source...
  39. Murashige, T., Skoog, F.: A revised medium for rapid growth and bioassays with tobacco tissue cultures. - Physiol. Plant. 15: 473-497, 1962. Go to original source...
  40. Murphy, A.S., Peer, W.A., Taiz, L.: Regulation of auxin transport by aminopeptidases and endogenous flavonoids. - Planta 211: 315-324, 2000. Go to original source...
  41. Murphy, A.S., Hoogner, K.R., Peer, W.A., Taiz, L.: Identification, purification and molecular cloning of N-1-naphthylphthalmic acid-binding plasma membraneassociated aminopeptides from Arabidopsis. - Plant Physiol. 128: 935-950, 2002. Go to original source...
  42. Parry, G., Delbarre, A., Marchant, A., Swarup, R., Napier, R., Perrot-Rechenmann, C., Bennett, M.J.: Novel auxin transport inhibitors phenocopy the auxin influx carrier mutation aux1. - Plant J. 25: 399-406, 2001. Go to original source...
  43. Peer, W.A., Bandyopadhyay, A., Blakeslee, J.J., Makam, S.N., Chen, R.J., Masson, P.H., Murphy, A.S.: Variation in expression and protein localization of the PIN family of auxin efflux facilitator proteins in flavonoid mutants with altered auxin transport in Arabidopsis thaliana. - Plant Cell 16: 1898-1911, 2004. Go to original source...
  44. Poupart, J., Waddell, C.S.: The rib1 mutant is resistant to indole-3-butyric acid, an endogenous auxin in Arabidopsis. - Plant Physiol. 124: 1739-1751, 2000. Go to original source...
  45. Poupart, J., Rashotte, A.M., Muday, G.K., Waddell, C.S.: The rib1 mutant of Arabidopsis has alterations in indole-3-butyric acid transport, hypocotyl elongation, and root architecture. - Plant Physiol. 139: 1460-1471, 2005. Go to original source...
  46. Rashotte, A.M., Poupart, J., Waddell, C.S., Muday, G.K.: Transport of the two natural auxins, indole-3-butyric acid and indole-3-acetic acid, in Arabidopsis. - Plant Physiol. 133: 761-772, 2003. Go to original source...
  47. Reinhardt, D., Mandel, T., Kuhlemeier, C.: Auxin regulates the initiation and radial position of plant lateral organs. - Plant Cell 12: 507-518, 2000. Go to original source...
  48. Rusak, G., Gutzeit, H.O., Ludwig-Müller, J.: Structurally related flavonoids with antioxidative properties differentially affect cell cycle progression and apoptosis of human acute leukemia cells. - Nutr. Res. 25: 143-155, 2005. Go to original source...
  49. Sabatini, S., Beis, D., Wolkenfelt, H., Murfett, J., Guilfoyle, T., Malamy, J., Benfey, P., Leyser, O., Bechtold, N., Weisbeek, P., Scheres, B.: An auxin-dependent distal organizer of pattern and polarity in the Arabidopsis root. - Cell 99: 463-472, 1999. Go to original source...
  50. Schwalm, K., Aloni, R., Langhans, M., Heller, W., Stich, S., Ullrich, C.I.: Flavonoid-related regulation of auxin accumulation in Agrobacterium tumefaciens-induced plant tumors. - Planta 218: 163-178, 2003. Go to original source...
  51. Swarup, R., Friml, J., Marchant, A., Ljung, K., Sandberg, G., Palme, K., Bennett, M.: Localization of the auxin permease AUX1 suggests two functionally distinct hormone transport pathways operate in the Arabidopsis root apex. - Genes Dev. 15: 2648-2653, 2001. Go to original source...
  52. Swarup, R., Marchant, A., Bennett, M.J.: Auxin transport: providing a sense of direction during plant development. - Biochem. Soc. Trans. 28: 481-485, 2000. Go to original source...
  53. Ulmasov, T., Murfett, J., Hagen, G., Guilfoyle, T.J.: Aux/lAA proteins repress expression of reporter genes containing natural and highly active synthetic auxin response elements. - Plant Cell 9: 1963-1971, 1997. Go to original source...
  54. Utsuno, K., Shikanai, T., Yamada, Y., Hashimoto, T.: AGR, an Agravitropic locus of Arabidopsis thaliana, encodes a novel membrane-protein family member. - Plant Cell Physiol. 39: 1111-1118, 1998. Go to original source...
  55. Wasson, A.P., Pellerone, F.I., Mathesius, U.: Silencing the flavonoid pathway in Medicago truncatula inhibits root nodule formation and prevents auxin transport regulation by Rhizobia. - Plant Cell 18: 1617-1629, 2006. Go to original source...
  56. Weijers, D., Sauer, M., Meurette, O., Friml, J., Ljung, K., Sandberg, G., Hooykaas, P., Offringa, R.: Maintenance of embryonic auxin distribution for apical-basal patterning by PIN-formed-dependent auxin transport in Arabidopsis. - Plant Cell 17: 2517-2526, 2005. Go to original source...
  57. Winkel-Shirley, B.: Flavonoid biosynthesis. a colorful model for genetics, biochemistry, cell biology, and biotechnology. - Plant Physiol. 126: 485-493, 2001a. Go to original source...
  58. Winkel-Shirley, B.: It takes a garden. How work on diverse plant species has contributed to an understanding of flavonoid metabolism. - Plant Physiol. 127: 1399-1404, 2001b. Go to original source...
  59. Woodward, A.W., Bartel, B.: Auxin: regulation, action and interaction. - Ann. Bot. 95: 707-735, 2005. Go to original source...
  60. Young, L.S., Harrison, B.R., Narayana, M., Moffatt, B.A., Gilroy, S., Masson, P.H.: Adenosine kinase modulates root gravitropism and cap morphogenesis in Arabidopsis. - Plant Physiol. 142: 564-573, 2006. Go to original source...
  61. Zazimalova, E., Napier, R.M.: Points of regulation for auxin action. - Plant Cell Rep. 21: 625-634, 2003. Go to original source...
  62. Zolman, B.K., Bartel, B.: An Arabidopsis indole-3-butyric acid-response mutant defective in PEROXIN6, an apparent ATPase implicated in peroxisomal function. - Proc. nat. Acad. Sci. USA 101: 1786-1791, 2004. Go to original source...
  63. Zolman, B.K., Monroe-Augustus, M., Thompson, B., Hawes, J.W., Krukenberg, K.A., Matsuda, S.P.T., Bartel, B.: chy1, an Arabidopsis mutant with impaired β-oxidation, is defective in a peroxisomal β-hydroxyisobutyryl-CoA hydrolase. - J. biol. Chem. 276: 31037-31046, 2001. Go to original source...
  64. Zolman, B.K., Yoder, A., Bartel, B.: Genetic analysis of indole-3-butyric acid response in Arabidopsis thaliana reveals four mutant classes. - Genetics 156: 1323-1337, 2000. Go to original source...